Wnt/β‑catenin signaling: Causes and treatment targets of drug resistance in colorectal cancer (Review)
- Authors:
- Gui-Xian Zhu
- Dian Gao
- Zhao-Zhao Shao
- Li Chen
- Wen-Jie Ding
- Qiong-Fang Yu
-
Affiliations: Department of Gastroenterology and Hepatology, Second Affiliated Hospital of Nanchang University, Nanchang, Jiangxi 330006, P.R. China, Department of Pathogen Biology and Immunology, Medical College of Nanchang University, Nanchang, Jiangxi 330006, P.R. China - Published online on: December 1, 2020 https://doi.org/10.3892/mmr.2020.11744
- Article Number: 105
-
Copyright: © Zhu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Keum N and Giovannucci E: Global burden of colorectal cancer: Emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol. 16:713–732. 2019. View Article : Google Scholar | |
Rawla P, Sunkara T and Barsouk A: Epidemiology of colorectal cancer: Incidence, mortality, survival, and risk factors. Prz Gastroenterol. 14:89–103. 2019. | |
Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global patterns and trends in colorectal cancer incidence and mortality. Gut. 66:683–691. 2017. View Article : Google Scholar | |
Marmol I, Sanchez-de-Diego C, Pradilla Dieste A, Cerrada E and Rodriguez Yoldi MJ: Colorectal carcinoma: A general overview and future perspectives in colorectal cancer. Int J Mol Sci. 18:1972017. View Article : Google Scholar | |
Calvert PM and Frucht H: The genetics of colorectal cancer. Ann Intern Med. 137:603–612. 2002. View Article : Google Scholar | |
Angarita FA, Feinberg AE, Feinberg SM, Riddell RH and McCart JA: Management of complex polyps of the colon and rectum. Int J Colorectal Dis. 33:115–129. 2018. View Article : Google Scholar | |
Blank A, Roberts DE II, Dawson H, Zlobec I and Lugli A: Tumor heterogeneity in primary colorectal cancer and corresponding metastases. Does the apple fall far from the tree? Front Med (Lausanne). 5:2342018. | |
Dahmus JD, Kotler DL, Kastenberg DM and Kistler CA: The gut microbiome and colorectal cancer: A review of bacterial pathogenesis. J Gastrointest Oncol. 9:769–777. 2018. View Article : Google Scholar | |
Jayasekara H, English DR, Haydon A, Hodge AM, Lynch BM, Rosty C, Williamson EJ, Clendenning M, Southey MC, Jenkins MA, et al: Associations of alcohol intake, smoking, physical activity and obesity with survival following colorectal cancer diagnosis by stage, anatomic site and tumor molecular subtype. Int J Cancer. 142:238–250. 2018. View Article : Google Scholar | |
Mehta A and Patel BM: Therapeutic opportunities in colon cancer: Focus on phosphodiesterase inhibitors. Life Sci. 230:150–161. 2019. View Article : Google Scholar | |
Salonga D, Danenberg KD, Johnson M, Metzger R, Groshen S, Tsao-Wei DD, Lenz HJ, Leichman CG, Leichman L, Diasio RB and Danenberg PV: Colorectal tumors responding to 5-fluorouracil have low gene expression levels of dihydropyrimidine dehydrogenase, thymidylate synthase, and thymidine phosphorylase. Clin Cancer Res. 6:1322–1327. 2000. | |
Showalter SL, Showalter TN, Witkiewicz A, Havens R, Kennedy EP, Hucl T, Kern SE, Yeo CJ and Brody JR: Evaluating the drug-target relationship between thymidylate synthase expression and tumor response to 5-fluorouracil. Is it time to move forward? Cancer Biol Ther. 7:986–994. 2008. View Article : Google Scholar | |
Yaffee P, Osipov A, Tan C, Tuli R and Hendifar A: Review of systemic therapies for locally advanced and metastatic rectal cancer. J Gastrointest Oncol. 6:185–200. 2015. | |
Cunningham D, Humblet Y, Siena S, Khayat D, Bleiberg H, Santoro A, Bets D, Mueser M, Harstrick A, Verslype C, et al: Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N Engl J Med. 351:337–345. 2004. View Article : Google Scholar | |
Van Cutsem E, Peeters M, Siena S, Humblet Y, Hendlisz A, Neyns B, Canon JL, Van Laethem JL, Maurel J, Richardson G, et al: Open-label phase III trial of panitumumab plus best supportive care compared with best supportive care alone in patients with chemotherapy-refractory metastatic colorectal cancer. J Clin Oncol. 25:1658–1664. 2007. View Article : Google Scholar | |
Hu T, Li Z, Gao CY and Cho CH: Mechanisms of drug resistance in colon cancer and its therapeutic strategies. World J Gastroenterol. 22:6876–6889. 2016. View Article : Google Scholar | |
Li YJ, Lei YH, Yao N, Wang CR, Hu N, Ye WC, Zhang DM and Chen ZS: Autophagy and multidrug resisitance in cancer. Chin J Cancer. 36:522017. View Article : Google Scholar | |
Thomas H and Coley HM: Overcoming multidrug resistance in cancer: An update on the clinical strategy of inhibiting p-glycoprotein. Cancer Control. 10:159–165. 2003. View Article : Google Scholar | |
Tredan O, Galmarini CM, Patel K and Tannock IF: Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst. 99:1441–1454. 2007. View Article : Google Scholar | |
Wang MY, Qiu YH, Cai ML, Zhang CH, Wang XW, Liu H, Chen Y, Zhao WL, Liu JB and Shao RG: Role and molecular mechanism of stem cells in colorectal cancer initiation. J Drug Target. 28:1–10. 2020. View Article : Google Scholar | |
Liu X, Fu Q, Du Y, Yang Y and Cho WC: MicroRNA as regulators of cancer stem cells and chemoresistance in colorectal cancer. Curr Cancer Drug Targets. 16:738–754. 2016. View Article : Google Scholar | |
Fanale D, Barraco N, Listi A, Bazan V and Russo A: Non-coding RNAs functioning in colorectal cancer stem cells. Adv Exp Med Biol. 937:93–108. 2016. View Article : Google Scholar | |
Rahmani F, Avan A, Hashemy SI and Hassanian SM: Role of Wnt/beta-catenin signaling regulatory microRNAs in the pathogenesis of colorectal cancer. J Cell Physiol. 233:811–817. 2018. View Article : Google Scholar | |
Das PK, Islam F and Lam AK: The roles of cancer stem cells and therapy resistance in colorectal carcinoma. Cells. 9:13922020. View Article : Google Scholar | |
Chikazawa N, Tanaka H, Tasaka T, Nakamura M, Tanaka M, Onishi H and Katano M: Inhibition of Wnt signaling pathway decreases chemotherapy-resistant side-population colon cancer cells. Anticancer Res. 30:2041–2048. 2010. | |
Shi L, Xi J, Xu X, Peng B and Zhang B: MiR-148a suppressed cell invasion and migration via targeting WNT10b and modulating β-catenin signaling in cisplatin-resistant colorectal cancer cells. Biomed Pharmacother. 109:902–909. 2019. View Article : Google Scholar | |
Hu YB, Yan C, Mu L, Mi YL, Zhao H, Hu H, Li XL, Tao DD, Wu YQ, Gong JP and Qin JC: Exosomal Wnt-induced dedifferentiation of colorectal cancer cells contributes to chemotherapy resistance. Oncogene. 38:1951–1965. 2019. View Article : Google Scholar | |
Nusse R and Varmus HE: Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell. 31:99–109. 1982. View Article : Google Scholar | |
Rijsewijk F, Schuermann M, Wagenaar E, Parren P, Weigel D and Nusse R: The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell. 50:649–657. 1987. View Article : Google Scholar | |
Kahn M: Can we safely target the WNT pathway? Nat Rev Drug Discov. 13:513–532. 2014. View Article : Google Scholar | |
Zeng ZY, Zhou YH, Zhang WL, Xiong W, Fan SQ, Li XL, Luo XM, Wu MH, Yang YX, Huang C, et al: Gene expression profiling of nasopharyngeal carcinoma reveals the abnormally regulated Wnt signaling pathway. Hum Pathol. 38:120–133. 2007. View Article : Google Scholar | |
Pate KT, Stringari C, Sprowl-Tanio S, Wang K, TeSlaa T, Hoverter NP, McQuade MM, Garner C, Digman MA, Teitell MA, et al: Wnt signaling directs a metabolic program of glycolysis and angiogenesis in colon cancer. EMBO J. 33:1454–1473. 2014. View Article : Google Scholar | |
Polakis P: Wnt signaling in cancer. Cold Spring Harb Perspect Biol. 4:a0080522012. View Article : Google Scholar | |
Tammela T, Sanchez-Rivera FJ, Cetinbas NM, Wu K, Joshi NS, Helenius K, Park Y, Azimi R, Kerper NR, Wesselhoeft RA, et al: A Wnt-producing niche drives proliferative potential and progression in lung adenocarcinoma. Nature. 545:355–359. 2017. View Article : Google Scholar | |
Lee SY, Jeon HM, Ju MK, Kim CH, Yoon G, Han SI, Park HG and Kang HS: Wnt/Snail signaling regulates cytochrome C oxidase and glucose metabolism. Cancer Res. 72:3607–3617. 2012. View Article : Google Scholar | |
Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR III and Nusse R: Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature. 423:448–452. 2003. View Article : Google Scholar | |
Takada R, Satomi Y, Kurata T, Ueno N, Norioka S, Kondoh H, Takao T and Takada S: Monounsaturated fatty acid modification of Wnt protein: Its role in Wnt secretion. Dev Cell. 11:791–801. 2006. View Article : Google Scholar | |
He B, You L, Uematsu K, Xu Z, Lee AY, Matsangou M, McCormick F and Jablons DM: A monoclonal antibody against Wnt-1 induces apoptosis in human cancer cells. Neoplasia. 6:7–14. 2004. View Article : Google Scholar | |
Chen G, Shukeir N, Potti A, Sircar K, Aprikian A, Goltzman D and Rabbani SA: Up-regulation of Wnt-1 and beta-catenin production in patients with advanced metastatic prostate carcinoma: Potential pathogenetic and prognostic implications. Cancer. 101:1345–1356. 2004. View Article : Google Scholar | |
Babaei K, Khaksar R, Zeinali T, Hemmati H, Bandegi A, Samidoust P, Ashoobi MT, Hashemian H, Delpasand K, Talebinasab F, et al: Epigenetic profiling of MUTYH, KLF6, WNT1 and KLF4 genes in carcinogenesis and tumorigenesis of colorectal cancer. Biomedicine (Taipei). 9:222019. View Article : Google Scholar | |
Jia S, Qu T, Feng M, Ji K, Li Z, Jiang W and Ji J: Association of Wnt1-inducible signaling pathway protein-1 with the proliferation, migration and invasion in gastric cancer cells. Tumour Biol. 39:10104283176997552017. View Article : Google Scholar | |
Bodnar L, Stanczak A, Cierniak S, Smoter M, Cichowicz M, Kozlowski W, Szczylik C, Wieczorek M and Lamparska-Przybysz M: Wnt/β-catenin pathway as a potential prognostic and predictive marker in patients with advanced ovarian cancer. J Ovarian Res. 7:162014. View Article : Google Scholar | |
Huang CB, Ma RJ, Xu Y, Li N, Li ZX, Yue J, Li HX, Guo Y and Qi D: Wnt2 promotes non-small cell lung cancer progression by activating WNT/β-catenin pathway. Am J Cancer Res. 5:1032–1046. 2015. | |
Katoh M: Frequent up-regulation of WNT2 in primary gastric cancer and colorectal cancer. Int J Oncol. 19:1003–1007. 2001. | |
Nakashima N, Liu D, Huang CL, Ueno M, Zhang X and Yokomise H: Wnt3 gene expression promotes tumor progression in non-small cell lung cancer. Lung Cancer. 76:228–234. 2012. View Article : Google Scholar | |
Wang HS, Nie X, Wu RB, Yuan HW, Ma YH, Liu XL, Zhang JY, Deng XL, Na Q, Jin HY, et al: Downregulation of human Wnt3 in gastric cancer suppresses cell proliferation and induces apoptosis. Onco Targets Ther. 9:3849–3860. 2016. View Article : Google Scholar | |
Nie XB, Xia FL, Liu Y, Zhou Y, Ye WL, Hean PH, Meng JM, Liu HY, Liu L, Wen JX, et al: Downregulation of Wnt3 suppresses colorectal cancer development through inhibiting cell proliferation and migration. Front Pharmacol. 10:11102019. View Article : Google Scholar | |
Thiago L, Costa ES, Lopes DV, Otazu IB, Nowill AE, Mendes FA, Portilho DM, Abreu JG, Mermelstein CS, Orfao A, et al: The Wnt signaling pathway regulates Nalm-16 b-cell precursor acute lymphoblastic leukemic cell line survival and etoposide resistance. Biomed Pharmacother. 64:63–72. 2010. View Article : Google Scholar | |
Zimmerman ZF, Kulikauskas RM, Bomsztyk K, Moon RT and Chien AJ: Activation of Wnt/β-catenin signaling increases apoptosis in melanoma cells treated with trail. PLoS One. 8:e695932013. View Article : Google Scholar | |
Annavarapu SR, Cialfi S, Dominici C, Kokai GK, Uccini S, Ceccarelli S, McDowell HP and Helliwell TR: Characterization of Wnt/β-catenin signaling in rhabdomyosarcoma. Lab Invest. 93:1090–1099. 2013. View Article : Google Scholar | |
Fox SA, Richards AK, Kusumah I, Perumal V, Bolitho EM, Mutsaers SE and Dharmarajan AM: Expression profile and function of Wnt signaling mechanisms in malignant mesothelioma cells. Biochem Biophys Res Commun. 440:82–87. 2013. View Article : Google Scholar | |
Wang SH, Li N, Wei Y, Li QR and Yu ZP: β-catenin deacetylation is essential for WNT-induced proliferation of breast cancer cells. Mol Med Rep. 9:973–978. 2014. View Article : Google Scholar | |
Akaboshi S, Watanabe S, Hino Y, Sekita Y, Xi Y, Araki K, Yamamura K, Oshima M, Ito T, Baba H and Nakao M: HMGA1 is induced by Wnt/beta-catenin pathway and maintains cell proliferation in gastric cancer. Am J Pathol. 175:1675–1685. 2009. View Article : Google Scholar | |
Zhao L, Wang LL, Zhang CL, Liu Z, Piao YJ, Yan J, Xiang R, Yao YQ and Y S: E6-induced selective translation of WNT4 and JIP2 promotes the progression of cervical cancer via a noncanonical WNT signaling pathway. Signal Transduct Target Ther. 4:322019. View Article : Google Scholar | |
McDonald SL and Silver A: The opposing roles of Wnt-5a in cancer. Br J Cancer. 101:209–214. 2009. View Article : Google Scholar | |
Li J, Ying J, Fan Y, Wu L, Ying Y, Chan AT, Srivastava G and Tao Q: WNT5A antagonizes WNT/β-catenin signaling and is frequently silenced by promoter CpG methylation in esophageal squamous cell carcinoma. Cancer Biol Ther. 10:617–624. 2010. View Article : Google Scholar | |
Ying J, Li H, Yu J, Ng KM, Poon FF, Wong SC, Chan AT, Sung JJ and Tao Q: WNT5A exhibits tumor-suppressive activity through antagonizing the Wnt/beta-catenin signaling, and is frequently methylated in colorectal cancer. Clin Cancer Res. 14:55–61. 2008. View Article : Google Scholar | |
Kremenevskaja N, von Wasielewski R, Rao AS, Schofl C, Andersson T and Brabant G: Wnt-5a has tumor suppressor activity in thyroid carcinoma. Oncogene. 24:2144–2154. 2005. View Article : Google Scholar | |
Thiele S, Rachner TD, Rauner M and Hofbauer LC: WNT5A and its receptors in the bone-cancer dialogue. J Bone Miner Res. 31:1488–1496. 2016. View Article : Google Scholar | |
Kurayoshi M, Oue N, Yamamoto H, Kishida M, Inoue A, Asahara T, Yasui W and Kikuchi A: Expression of Wnt-5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion. Cancer Res. 66:10439–10448. 2006. View Article : Google Scholar | |
Huang CL, Liu D, Nakano J, Ishikawa S, Kontani K, Yokomise H and Ueno M: Wnt5a expression is associated with the tumor proliferation and the stromal vascular endothelial growth factor-an expression in non-small-cell lung cancer. J Clin Oncol. 23:8765–8773. 2005. View Article : Google Scholar | |
Bo H, Zhang S, Gao L, Chen Y, Zhang J, Chang X and Zhu M: Upregulation of Wnt5a promotes epithelial-tomesenchymal transition and metastasis of pancreatic cancer cells. BMC Cancer. 13:4962013. View Article : Google Scholar | |
Navarrete-Meneses MDP and Perez-Vera P: Epigenetic alterations in acute lymphoblastic leukemia. Bol Med Hosp Infant Mex. 74:243–264. 2017.(In Spanish). | |
Stewart DJ: Wnt signaling pathway in non-small cell lung cancer. J Natl Cancer Inst. 106:djt3562014. View Article : Google Scholar | |
Kirikoshi H and Katoh M: Expression of WNT7A in human normal tissues and cancer, and regulation of WNT7A and WNT7B in human cancer. Int J Oncol. 21:895–900. 2002. | |
Vesel M, Rapp J, Feller D, Kiss E, Jaromi L, Meggyes M, Miskei G, Duga B, Smuk G, Laszlo T, et al: ABCB1 and ABCG2 drug transporters are differentially expressed in non-small cell lung cancers (NSCLC) and expression is modified by cisplatin treatment via altered Wnt signaling. Respir Res. 18:522017. View Article : Google Scholar | |
Li J, Zhang Z, Wang L and Zhang Y: The oncogenic role of Wnt10a in colorectal cancer through activation of canonical Wnt/β-catenin signaling. Oncol Lett. 17:3657–3664. 2019. | |
Li P, Liu W, Xu Q and Wang C: Clinical significance and biological role of Wnt10a in ovarian cancer. Oncol Lett. 14:6611–6617. 2017. | |
Hsu RJ, Ho JY, Cha TL, Yu DS, Wu CL, Huang WP, Chu P, Chen YH, Chen JT and Yu CP: WNT10A plays an oncogenic role in renal cell carcinoma by activating WNT/beta-catenin pathway. PLoS One. 7:e476492012. View Article : Google Scholar | |
Kirikoshi H, Inoue S, Sekihara H and Katoh M: Expression of WNT10A in human cancer. Int J Oncol. 19:997–1001. 2001. | |
Dong T, Zhang Z, Zhou W, Zhou X, Geng C, Chang LK, Tian X and Liu S: WNT10A/β-catenin pathway in tumorigenesis of papillary thyroid carcinoma. Oncol Rep. 38:1287–1294. 2017. View Article : Google Scholar | |
Wend P, Runke S, Wend K, Anchondo B, Yesayan M, Jardon M, Hardie N, Loddenkemper C, Ulasov I, Lesniak MS, et al: WNT10B/beta-catenin signalling induces HMGA2 and proliferation in metastatic triple-negative breast cancer. EMBO Mol Med. 5:264–279. 2013. View Article : Google Scholar | |
Chen H, Wang Y and Xue F: Expression and the clinical significance of Wnt10a and Wnt10b in endometrial cancer are associated with the Wnt/β-catenin pathway. Oncol Rep. 29:507–514. 2013. View Article : Google Scholar | |
Saitoh T, Kirikoshi H, Mine T and Katoh M: Proto-oncogene WNT10B is up-regulated by tumor necrosis factor alpha in human gastric cancer cell line MKN45. Int J Oncol. 19:1187–1192. 2001. | |
Bartis D, Csongei V, Weich A, Kiss E, Barko S, Kovacs T, Avdicevic M, D'Souza VK, Rapp J, Kvell K, et al: Down-regulation of canonical and up-regulation of non-canonical Wnt signalling in the carcinogenic process of squamous cell lung carcinoma. PLoS One. 8:e573932013. View Article : Google Scholar | |
Tian S, Hu J, Tao K, Wang J, Chu Y, Li J, Liu Z, Ding X, Xu L, Li Q, et al: Secreted AGR2 promotes invasion of colorectal cancer cells via Wnt11-mediated non-canonical Wnt signaling. Exp Cell Res. 364:198–207. 2018. View Article : Google Scholar | |
Toyama T, Lee HC, Koga H, Wands JR and Kim M: Noncanonical Wnt11 inhibits hepatocellular carcinoma cell proliferation and migration. Mol Cancer Res. 8:254–265. 2010. View Article : Google Scholar | |
Yin P, Wang W, Zhang Z, Bai Y, Gao J and Zhao C: Wnt signaling in human and mouse breast cancer: Focusing on Wnt ligands, receptors and antagonists. Cancer Sci. 109:3368–3375. 2018. View Article : Google Scholar | |
Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ and Clevers H: Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 449:1003–1007. 2007. View Article : Google Scholar | |
Bourroul GM, Fragoso HJ, Gomes JW, Bourroul VS, Oshima CT, Gomes TS, Saba GT, Palma RT and Waisberg J: The destruction complex of beta-catenin in colorectal carcinoma and colonic adenoma. Einstein (Sao Paulo). 14:135–142. 2016. View Article : Google Scholar | |
Sawa M, Masuda M and Yamada T: Targeting the Wnt signaling pathway in colorectal cancer. Expert Opin Ther Targets. 20:419–429. 2016. View Article : Google Scholar | |
Amit S, Hatzubai A, Birman Y, Andersen JS, Ben-Shushan E, Mann M, Ben-Neriah Y and Alkalay I: Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: A molecular switch for the Wnt pathway. Genes Dev. 16:1066–1076. 2002. View Article : Google Scholar | |
He X, Semenov M, Tamai K and Zeng X: LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: Arrows point the way. Development. 131:1663–1677. 2004. View Article : Google Scholar | |
Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M and Niehrs C: Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science. 316:1619–1622. 2007. View Article : Google Scholar | |
Zarkou V, Galaras A, Giakountis A and Hatzis P: Crosstalk mechanisms between the WNT signaling pathway and long non-coding RNAs. Noncoding RNA Res. 3:42–53. 2018. View Article : Google Scholar | |
Hammond WA, Swaika A and Mody K: Pharmacologic resistance in colorectal cancer: A review. Ther Adv Med Oncol. 8:57–84. 2016. View Article : Google Scholar | |
Gheidari F, Bakhshandeh B, Teimoori-Toolabi L, Mehrtash A, Ghadir M and Zeinali S: TCF4 silencing sensitizes the colon cancer cell line to oxaliplatin as a common chemotherapeutic drug. Anticancer Drugs. 25:908–916. 2014. View Article : Google Scholar | |
Kosuri KV, Wu X, Wang L, Villalona-Calero MA and Otterson GA: An epigenetic mechanism for capecitabine resistance in mesothelioma. Biochem Biophys Res Commun. 391:1465–1470. 2010. View Article : Google Scholar | |
Rieth J and Subramanian S: Mechanisms of intrinsic tumor resistance to immunotherapy. Int J Mol Sci. 19:13402018. View Article : Google Scholar | |
Ghadimi BM, Grade M, Difilippantonio MJ, Varma S, Simon R, Montagna C, Fuzesi L, Langer C, Becker H, Liersch T and Ried T: Effectiveness of gene expression profiling for response prediction of rectal adenocarcinomas to preoperative chemoradiotherapy. J Clin Oncol. 23:1826–1838. 2005. View Article : Google Scholar | |
Emons G, Spitzner M, Reineke S, Moller J, Auslander N, Kramer F, Hu Y, Beissbarth T, Wolff HA, Rave-Frank M, et al: Chemoradiotherapy resistance in colorectal cancer cells is mediated by Wnt/beta-catenin signaling. Mol Cancer Res. 15:1481–1490. 2017. View Article : Google Scholar | |
Deng YH, Pu XX, Huang MJ, Xiao J, Zhou JM, Lin TY and Lin EH: 5-Fluorouracil upregulates the activity of Wnt signaling pathway in CD133-positive colon cancer stem-like cells. Chin J Cancer. 29:810–815. 2010. View Article : Google Scholar | |
Vaish V, Kim J and Shim M: Jagged-2 (JAG2) enhances tumorigenicity and chemoresistance of colorectal cancer cells. Oncotarget. 8:53262–53275. 2017. View Article : Google Scholar | |
Kukcinaviciute E, Jonusiene V, Sasnauskiene A, Dabkeviciene D, Eidenaite E and Laurinavicius A: Significance of Notch and Wnt signaling for chemoresistance of colorectal cancer cells HCT116. J Cell Biochem. 119:5913–5920. 2018. View Article : Google Scholar | |
Gonzalez-Exposito R, Semiannikova M, Griffiths B, Khan K, Barber LJ, Woolston A, Spain G, von Loga K, Challoner B, Patel R, et al: CEA expression heterogeneity and plasticity confer resistance to the CEA-targeting bispecific immunotherapy antibody cibisatamab (CEA-TCB) in patient-derived colorectal cancer organoids. J Immunother Cancer. 7:1012019. View Article : Google Scholar | |
Chang TC, Yeh CT, Adebayo BO, Lin YC, Deng L, Rao YK, Huang CC, Lee WH, Wu AT, Hsiao M, et al: 4-Acetylantroquinonol B inhibits colorectal cancer tumorigenesis and suppresses cancer stem-like phenotype. Toxicol Appl Pharmacol. 288:258–268. 2015. View Article : Google Scholar | |
Vermeulen L, Sprick MR, Kemper K, Stassi G and Medema JP: Cancer stem cells-old concepts, new insights. Cell Death Differ. 15:947–958. 2008. View Article : Google Scholar | |
Munro MJ, Wickremesekera SK, Peng L, Tan ST and Itinteang T: Cancer stem cells in colorectal cancer: A review. J Clin Pathol. 71:110–116. 2018. View Article : Google Scholar | |
Li N, Babaei-Jadidi R, Lorenzi F, Spencer-Dene B, Clarke P, Domingo E, Tulchinsky E, Vries RGJ, Kerr D, Pan Y, et al: An FBXW7-ZEB2 axis links EMT and tumour microenvironment to promote colorectal cancer stem cells and chemoresistance. Oncogenesis. 8:132019. View Article : Google Scholar | |
Prieti-Vila M, Takahashi R, Usuba W, Kohama I and Ochiya T: Drug resistance driven by cancer stem cells and their niche. Int J Mol Sci. 18:25742017. View Article : Google Scholar | |
Li L and Xie T: Stem cell niche: Structure and function. Annu Rev Cell Dev Biol. 21:605–631. 2005. View Article : Google Scholar | |
Liu H, Zhang W, Jia Y, Yu Q, Grau GE, Peng L, Ran Y, Yang Z, Deng H and Lou J: Single-cell clones of liver cancer stem cells have the potential of differentiating into different types of tumor cells. Cell Death Dis. 4:e8572013. View Article : Google Scholar | |
Daverey A, Drain AP and Kidambi S: Physical intimacy of breast cancer cells with mesenchymal stem cells elicits trastuzumab resistance through src activation. Sci Rep. 5:137442015. View Article : Google Scholar | |
Kim JY, Lee HY, Park KK, Choi YK, Nam JS and Hong IS: CWP232228 targets liver cancer stem cells through Wnt/β-catenin signaling: A novel therapeutic approach for liver cancer treatment. Oncotarget. 7:20395–20409. 2016. View Article : Google Scholar | |
Fevr T, Robine S, Louvard D and Huelsken J: Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol Cell Biol. 27:7551–7559. 2007. View Article : Google Scholar | |
Dahal Lamichane B, Jung SY, Yun J, Kang S, Kim DY, Lamichane S, Kim YJ, Park JH, Jang WB, Ji ST, et al: AGR2 is a target of canonical Wnt/β-catenin signaling and is important for stemness maintenance in colorectal cancer stem cells. Biochem Biophys Res Commun. 515:600–606. 2019. View Article : Google Scholar | |
Liu YS, Hsu HC, Tseng KC, Chen HC and Chen SJ: Lgr5 promotes cancer stemness and confers chemoresistance through ABCB1 in colorectal cancer. Biomed Pharmacother. 67:791–799. 2013. View Article : Google Scholar | |
Zhan T, Ambrosi G, Wandmacher AM, Rauscher B, Betge J, Rindtorff N, Haussler RS, Hinsenkamp I, Bamberg L, Hessling B, et al: MEK inhibitors activate Wnt signalling and induce stem cell plasticity in colorectal cancer. Nat Commun. 10:21972019. View Article : Google Scholar | |
Wu W, Cao J, Ji Z, Wang J, Jiang T and Ding H: Co-expression of Lgr5 and CXCR4 characterizes cancer stem-like cells of colorectal cancer. Oncotarget. 7:81144–81155. 2016. View Article : Google Scholar | |
Kobayashi S, Yamada-Okabe H, Suzuki M, Natori O, Kato A, Matsubara K, Jau Chen Y, Yamazaki M, Funahashi S, Yoshida K, et al: LGR5-positive colon cancer stem cells interconvert with drug-resistant LGR5-negative cells and are capable of tumor reconstitution. Stem Cells. 30:2631–2644. 2012. View Article : Google Scholar | |
Villanueva-Toledo J, Ponciano-Gomez A, Ortiz-Sanchez E and Garrido E: Side populations from cervical-cancer-derived cell lines have stem-cell-like properties. Mol Biol Rep. 41:1993–2004. 2014. View Article : Google Scholar | |
Steinbichler TB, Dudas J, Skvortsov S, Ganswindt U, Riechelmann H and Skvortsova II: Therapy resistance mediated by cancer stem cells. Semin Cancer Biol. 53:156–167. 2018. View Article : Google Scholar | |
Singh A and Settleman J: EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene. 29:4741–4751. 2010. View Article : Google Scholar | |
Martin-Orozco E, Sanchez-Fernandez A, Ortiz-Parra I and Ayala-San Nicolas M: WNT signaling in tumors: The way to evade drugs and immunity. Front Immunol. 10:28542019. View Article : Google Scholar | |
Islam MO, Kanemura Y, Tajria J, Mori H, Kobayashi S, Shofuda T, Miyake J, Hara M, Yamasaki M and Okano H: Characterization of ABC transporter ABCB1 expressed in human neural stem/progenitor cells. FEBS Lett. 579:3473–3480. 2005. View Article : Google Scholar | |
Falasca M and Linton KJ: Investigational ABC transporter inhibitors. Expert Opin Investig Drugs. 21:657–666. 2012. View Article : Google Scholar | |
Duan Z, Li X, Huang H, Yuan W, Zheng SL, Liu X, Zhang Z, Choy E, Harmon D, Mankin H and Hornicek F: Synthesis and evaluation of (2-(4-methoxyphenyl)-4-quinolinyl)(2-piperidinyl)methanol (NSC23925) isomers to reverse multidrug resistance in cancer. J Med Chem. 55:3113–3121. 2012. View Article : Google Scholar | |
Huang XC, Sun YL, Salim AA, Chen ZS and Capon RJ: Parguerenes: Marine red alga bromoditerpenes as inhibitors of P-glycoprotein (ABCB1) in multidrug resistant human cancer cells. Biochem Pharmacol. 85:1257–1268. 2013. View Article : Google Scholar | |
Zinzi L, Contino M, Cantore M, Capparelli E, Leopoldo M and Colabufo NA: ABC transporters in CSCs membranes as a novel target for treating tumor relapse. Front Pharmacol. 5:1632014. View Article : Google Scholar | |
Liu YY, Gupta V, Patwardhan GA, Bhinge K, Zhao Y, Bao J, Mehendale H, Cabot MC, Li YT and Jazwinski SM: Glucosylceramide synthase upregulates MDR1 expression in the regulation of cancer drug resistance through cSrc and beta-catenin signaling. Mol Cancer. 9:1452010. View Article : Google Scholar | |
Kugimiya N, Nishimoto A, Hosoyama T, Ueno K, Enoki T, Li TS and Hamano K: The c-MYC-ABCB5 axis plays a pivotal role in 5-fluorouracil resistance in human colon cancer cells. J Cell Mol Med. 19:1569–1581. 2015. View Article : Google Scholar | |
Wang T, Chen Z, Zhu Y, Pan Q, Liu Y, Qi X, Jin L, Jin J, Ma X and Hua D: Inhibition of transient receptor potential channel 5 reverses 5-Fluorouracil resistance in human colorectal cancer cells. J Biol Chem. 290:448–456. 2015. View Article : Google Scholar | |
Plaks V, Kong N and Werb Z: The cancer stem cell niche: How essential is the niche in regulating stemness of tumor cells? Cell Stem Cell. 16:225–238. 2015. View Article : Google Scholar | |
Osthus RC, Shim H, Kim S, Li Q, Reddy R, Mukherjee M, Xu Y, Wonsey D, Lee LA and Dang CV: Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem. 275:21797–21800. 2000. View Article : Google Scholar | |
Wang T, Ning K, Lu TX and Hua D: Elevated expression of TrpC5 and GLUT1 is associated with chemoresistance in colorectal cancer. Oncol Rep. 37:1059–1065. 2017. View Article : Google Scholar | |
Matsui M and Corey DR: Non-coding RNAs as drug targets. Nat Rev Drug Discov. 16:167–179. 2017. View Article : Google Scholar | |
Ling H, Fabbri M and Calin GA: MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat Rev Drug Discov. 12:847–865. 2013. View Article : Google Scholar | |
Laurent GS, Wahlestedt C and Kapranov P: The landscape of long noncoding RNA classification. Trends Genet. 31:239–251. 2015. View Article : Google Scholar | |
Sato-Kuwabara Y, Melo SA, Soares FA and Calin GA: The fusion of two worlds: Non-coding RNAs and extracellular vesicles-diagnostic and therapeutic implications (Review). Int J Oncol. 46:17–27. 2015. View Article : Google Scholar | |
Ebbesen KK, Kjems J and Hansen TB: Circular RNAs: Identification, biogenesis and function. Biochim Biophys Acta. 1859:163–168. 2016. View Article : Google Scholar | |
Chen HY, Lang YD, Lin HN, Liu YR, Liao CC, Nana AW, Yen Y and Chen RH: miR-103/107 prolong Wnt/β-catenin signaling and colorectal cancer stemness by targeting Axin2. Sci Rep. 9:96872019. View Article : Google Scholar | |
Zhou H, Lin C, Zhang Y, Zhang X, Zhang C, Zhang P, Xie X and Ren Z: miR-506 enhances the sensitivity of human colorectal cancer cells to oxaliplatin by suppressing MDR1/P-gp expression. Cell Prolif. 50:e123412017. View Article : Google Scholar | |
Lu ML, Zhang Y, Li J, Fu Y, Li WH, Zhao GF, Li XH, Wei L, Liu GB and Huang H: MicroRNA-124 inhibits colorectal cancer cell proliferation and suppresses tumor growth by interacting with PLCB1 and regulating Wnt/β-catenin signaling pathway. Eur Rev Med Pharmacol Sci. 23:121–136. 2019. | |
Liang CQ, Fu YM, Liu ZY, Xing BR, Jin Y and Huang JL: The effect of miR-224 down-regulation on SW80 cell proliferation and apoptosis and weakening of ADM drug resistance. Eur Rev Med Pharmacol Sci. 21:5008–5016. 2017. | |
Lucero OM, Dawson DW, Moon RT and Chien AJ: A re-evaluation of the ‘oncogenic’ nature of Wnt/beta-catenin signaling in melanoma and other cancers. Curr Oncol Rep. 12:314–318. 2010. View Article : Google Scholar | |
Song C, Lu P, Sun G, Yang L and Wang Z and Wang Z: miR-34a sensitizes lung cancer cells to cisplatin via p53/miR-34a/MYCN axis. Biochem Biophys Res Commun. 482:22–27. 2017. View Article : Google Scholar | |
Schulz-Heddergott R, Stark N, Edmunds SJ, Li J, Conradi LC, Bohnenberger H, Ceteci F, Greten FR, Dobbelstein M and Moll UM: Therapeutic ablation of gain-of-function mutant p53 in colorectal cancer inhibits stat3-mediated tumor growth and invasion. Cancer Cell. 34:298–314 e297. 2018. View Article : Google Scholar | |
Nakayama M, Sakai E, Echizen K, Yamada Y, Oshima H, Han TS, Ohki R, Fujii S, Ochiai A, Robine S, et al: Intestinal cancer progression by mutant p53 through the acquisition of invasiveness associated with complex glandular formation. Oncogene. 36:5885–5896. 2017. View Article : Google Scholar | |
Lane DP, Cheok CF and Lain S: p53-based cancer therapy. Cold Spring Harb Perspect Biol. 2:a0012222010. View Article : Google Scholar | |
Tsou SH, Hou MH, Hsu LC, Chen TM and Chen YH: Gain-of-function p53 mutant with 21-bp deletion confers susceptibility to multidrug resistance in MCF-7 cells. Int J Mol Med. 37:233–242. 2016. View Article : Google Scholar | |
Li XL, Zhou J, Chen ZR and Chng WJ: P53 mutations in colorectal cancer-molecular pathogenesis and pharmacological reactivation. World J Gastroenterol. 21:84–93. 2015. View Article : Google Scholar | |
Kwak B, Kim DU, Kim TO, Kim HS and Kim SW: MicroRNA-552 links Wnt signaling to p53 tumor suppressor in colorectal cancer. Int J Oncol. 53:1800–1808. 2018. | |
Zhou AD, Diao LT, Xu H, Xiao ZD, Li JH, Zhou H and Qu LH: β-Catenin/LEF1 transactivates the microRNA-371-373 cluster that modulates the Wnt/β-catenin-signaling pathway. Oncogene. 31:2968–2978. 2012. View Article : Google Scholar | |
Wang LQ, Yu P, Li B, Guo YH, Liang ZR, Zheng LL, Yang JH, Xu H, Liu S, Zheng LS, et al: miR-372 and miR-373 enhance the stemness of colorectal cancer cells by repressing differentiation signaling pathways. Mol Oncol. 12:1949–1964. 2018. View Article : Google Scholar | |
Han P, Li JW, Zhang BM, Lv JC, Li YM, Gu XY, Yu ZW, Jia YH, Bai XF, Li L, et al: The lncRNA CRNDE promotes colorectal cancer cell proliferation and chemoresistance via miR-181a-5p-mediated regulation of Wnt/β-catenin signaling. Mol Cancer. 16:92017. View Article : Google Scholar | |
Xiao Z, Qu Z, Chen Z, Fang Z, Zhou K, Huang Z, Guo X and Zhang Y: LncRNA HOTAIR is a prognostic biomarker for the proliferation and chemoresistance of colorectal cancer via MiR-203a-3p-mediated Wnt/ß-catenin signaling pathway. Cell Physiol Biochem. 46:1275–1285. 2018. View Article : Google Scholar | |
Wu KF, Liang WC, Feng L, Pang JX, Waye MM, Zhang JF and Fu WM: H19 mediates methotrexate resistance in colorectal cancer through activating Wnt/β-catenin pathway. Exp Cell Res. 350:312–317. 2017. View Article : Google Scholar | |
Deng X, Ruan H, Zhang X, Xu X, Zhu Y, Peng H, Zhang X, Kong F and Guan M: Long noncoding RNA CCAL transferred from fibroblasts by exosomes promotes chemoresistance of colorectal cancer cells. Int J Cancer. 146:1700–1716. 2020. View Article : Google Scholar | |
Ma Y, Yang Y, Wang F, Moyer MP, Wei Q, Zhang P, Yang Z, Liu W, Zhang H, Chen N, et al: Long non-coding RNA CCAL regulates colorectal cancer progression by activating Wnt/β-catenin signalling pathway via suppression of activator protein 2α. Gut. 65:1494–1504. 2016. View Article : Google Scholar | |
Hanahan D and Coussens LM: Accessories to the crime: Functions of cells recruited to the tumor microenvironment. Cancer Cell. 21:309–322. 2012. View Article : Google Scholar | |
Sun Y: Tumor microenvironment and cancer therapy resistance. Cancer Lett. 380:205–215. 2016. View Article : Google Scholar | |
Castellone MD, Teramoto H, Williams BO, Druey KM and Gutkind JS: Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis. Science. 310:1504–1510. 2005. View Article : Google Scholar | |
Yang L, Lin C and Liu ZR: P68 RNA helicase mediates PDGF-induced epithelial mesenchymal transition by displacing Axin from beta-catenin. Cell. 127:139–155. 2006. View Article : Google Scholar | |
Gupta GP and Massague J: Cancer metastasis: Building a framework. Cell. 127:679–695. 2006. View Article : Google Scholar | |
Gross JC, Chaudhary V, Bartscherer K and Boutros M: Active Wnt proteins are secreted on exosomes. Nat Cell Biol. 14:1036–1045. 2012. View Article : Google Scholar | |
Hu JL, Wang W, Lan XL, Zeng ZC, Liang YS, Yan YR, Song FY, Wang FF, Zhu XH, Liao WJ, et al: CAFs secreted exosomes promote metastasis and chemotherapy resistance by enhancing cell stemness and epithelial-mesenchymal transition in colorectal cancer. Mol Cancer. 18:912019. View Article : Google Scholar | |
Xu X, Chang W, Yuan J, Han X, Tan X, Ding Y, Luo Y, Cai H, Liu Y, Gao X, et al: Periostin expression in intra-tumoral stromal cells is prognostic and predictive for colorectal carcinoma via creating a cancer-supportive niche. Oncotarget. 7:798–813. 2016. View Article : Google Scholar | |
Sun Y, Campisi J, Higano C, Beer TM, Porter P, Coleman I, True L and Nelson PS: Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med. 18:1359–1368. 2012. View Article : Google Scholar | |
Sun Y, Zhu D, Chen F, Qian M, Wei H, Chen W and Xu J: SFRP2 augments WNT16B signaling to promote therapeutic resistance in the damaged tumor microenvironment. Oncogene. 35:4321–4334. 2016. View Article : Google Scholar | |
Izumi D, Toden S, Ureta E, Ishimoto T, Baba H and Goel A: TIAM1 promotes chemoresistance and tumor invasiveness in colorectal cancer. Cell Death Dis. 10:2672019. View Article : Google Scholar | |
Takada K, Zhu D, Bird GH, Sukhdeo K, Zhao JJ, Mani M, Lemieux M, Carrasco DE, Ryan J, Horst D, et al: Targeted disruption of the BCL9/β-catenin complex inhibits oncogenic Wnt signaling. Sci Transl Med. 4:148ra1172012. View Article : Google Scholar | |
Tan Z, Huang Q, Zang J, Teng SF, Chen TR, Wei HF, Song DW, Liu TL, Yang XH, Fu CG, et al: HIF-1α activates hypoxia-induced BCL-9 expression in human colorectal cancer cells. Oncotarget. 8:25885–25896. 2017. View Article : Google Scholar | |
Wu X, Gu Z, Chen Y, Chen B, Chen W, Weng L and Liu X: Application of PD-1 blockade in cancer immunotherapy. Comput Struct Biotechnol J. 17:661–674. 2019. View Article : Google Scholar | |
Yaghoubi N, Soltani A, Ghazvini K, Hassanian SM and Hashemy SI: PD-1/PD-L1 blockade as a novel treatment for colorectal cancer. Biomed Pharmacother. 110:312–318. 2019. View Article : Google Scholar | |
Payandeh Z, Khalili S, Somi MH, Mard-Soltani M, Baghbanzadeh A, Hajiasgharzadeh K, Samadi N and Baradaran B: PD-1/PD-L1-dependent immune response in colorectal cancer. J Cell Physiol. 235:5461–5475. 2020. View Article : Google Scholar | |
Topalian SL, Taube JM, Anders RA and Pardoll DM: Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer. 16:275–287. 2016. View Article : Google Scholar | |
Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, et al: Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 313:1960–1964. 2006. View Article : Google Scholar | |
Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, et al: PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 515:568–571. 2014. View Article : Google Scholar | |
Spranger S, Koblish HK, Horton B, Scherle PA, Newton R and Gajewski TF: Mechanism of tumor rejection with doublets of CTLA-4, PD-1/PD-L1, or IDO blockade involves restored IL-2 production and proliferation of CD8+ T cells directly within the tumor microenvironment. J Immunother Cancer. 2:32014. View Article : Google Scholar | |
Spranger S, Dai D, Horton B and Gajewski TF: Tumor-residing Batf3 dendritic cells are required for effector t cell trafficking and adoptive t cell therapy. Cancer Cell. 31:711–723. 2017. View Article : Google Scholar | |
Feng M, Jin JQ, Xia L, Xiao T, Mei S, Wang X, Huang X, Chen J, Liu M, Chen C, et al: Pharmacological inhibition of β-catenin/BCL9 interaction overcomes resistance to immune checkpoint blockades by modulating T reg. Sci Adv. 5:eaau52402019. View Article : Google Scholar | |
Bottcher JP and Reis e Sousa C: The role of type 1 conventional dendritic cells in cancer immunity. Trends Cancer. 4:784–792. 2018. View Article : Google Scholar | |
Liu K and Li J, Wu X, Chen M, Luo F and Li J: GSK-3β inhibitor 6-bromo-indirubin-3′-oxime promotes both adhesive activity and drug resistance in colorectal cancer cells. Int J Oncol. 51:1821–1830. 2017. View Article : Google Scholar | |
Yan L, Yu HH, Liu YS, Wang YS and Zhao WH: Esculetin enhances the inhibitory effect of 5-Fluorouracil on the proliferation, migration and epithelial-mesenchymal transition of colorectal cancer. Cancer Biomark. 24:231–240. 2019. View Article : Google Scholar | |
Cai MH, Xu XG, Yan SL, Sun Z, Ying Y, Wang BK and Tu YX: Regorafenib suppresses colon tumorigenesis and the generation of drug resistant cancer stem-like cells via modulation of miR-34a associated signaling. J Exp Clin Cancer Res. 37:1512018. View Article : Google Scholar | |
Siraj AK, Kumar Parvathareddy S, Pratheeshkumar P, Padmaja Divya S, Ahmed SO, Melosantos R, Begum R, Concepcion R, Al-Sanea N, Ashari LH, et al: APC truncating mutations in middle eastern population: Tankyrase inhibitor is an effective strategy to sensitize APC mutant CRC To 5-FU chemotherapy. Biomed Pharmacother. 121:1095722020. View Article : Google Scholar | |
Wang J, Min H, Hu B, Xue X and Liu Y: Guanylate-binding protein-2 inhibits colorectal cancer cell growth and increases the sensitivity to paclitaxel of paclitaxel-resistant colorectal cancer cells by interfering Wnt signaling. J Cell Biochem. 121:1250–1259. 2020. View Article : Google Scholar | |
Wu CE, Zhuang YW, Zhou JY, Liu SL, Wang RP and Shu P: Cinnamaldehyde enhances apoptotic effect of oxaliplatin and reverses epithelial-mesenchymal transition and stemnness in hypoxic colorectal cancer cells. Exp Cell Res. 383:1115002019. View Article : Google Scholar | |
Zhao B, Wang L, Qiu H, Zhang M, Sun L, Peng P, Yu Q and Yuan X: Mechanisms of resistance to anti-EGFR therapy in colorectal cancer. Oncotarget. 8:3980–4000. 2017. View Article : Google Scholar | |
Sansom OJ, Meniel V, Wilkins JA, Cole AM, Oien KA, Marsh V, Jamieson TJ, Guerra C, Ashton GH, Barbacid M and Clarke AR: Loss of Apc allows phenotypic manifestation of the transforming properties of an endogenous K-ras oncogene in vivo. Proc Natl Acad Sci USA. 103:14122–14127. 2006. View Article : Google Scholar | |
He L, Zhu H, Zhou S, Wu T, Wu H, Yang H, Mao H, SekharKathera C, Janardhan A, Edick AM, et al: Wnt pathway is involved in 5-FU drug resistance of colorectal cancer cells. Exp Mol Med. 50:1012018. View Article : Google Scholar | |
Zhao Q, Zhuang K, Han K, Tang H, Wang Y, Si W and Yang Z: Silencing DVL3 defeats MTX resistance and attenuates stemness via Notch signaling pathway in colorectal cancer. Pathol Res Pract. 216:1529642020. View Article : Google Scholar | |
Zhang F, Sun H, Zhang S, Yang X, Zhang G and Su T: Overexpression of PER3 inhibits self-renewal capability and chemoresistance of colorectal cancer stem-like cells via inhibition of notch and β-catenin signaling. Oncol Res. 25:709–719. 2017. View Article : Google Scholar |